Phosphodiesterase 4 inhibition impairs cocaine-induced inhibitory synaptic plasticity and conditioned place preference

Neuropsychopharmacology

Volumn 37, Issue 11, 2012, Pages 2377-2387

  Zhong, Peng ^a   Wang, Wei ^a   Yu, Fei ^a   Nazari, Maressa ^a   Liu, Xiaojie ^a   Liu, Qing Song ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

cAMP response element binding protein (CREB); conditioned place preference (CPP); endocannabinoid; long term depression of inhibitory synaptic transmission (I LTD); phosphodiesterase 4 (PDE4)

Indexed keywords

4 (3 BUTOXY 4 METHOXYBENZYL) 2 IMIDAZOLIDINONE; CANNABINOID 1 RECEPTOR; COCAINE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DOPAMINE 2 RECEPTOR; PHOSPHODIESTERASE IV; ROLIPRAM;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; COCAINE DEPENDENCE; CONTROLLED STUDY; ENZYME INHIBITION; INHIBITORY SYNAPTIC PLASTICITY; MALE; NERVE CELL PLASTICITY; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; VENTRAL TEGMENTUM;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; COCAINE; CONDITIONING, OPERANT; CREB-BINDING PROTEIN; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 4; DOPAMINE; DOPAMINE UPTAKE INHIBITORS; DRUG ADMINISTRATION ROUTES; DRUG INTERACTIONS; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MICROINJECTIONS; NEURAL INHIBITION; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TYROSINE 3-MONOOXYGENASE; VALINE; VENTRAL TEGMENTAL AREA;

EID: 84866412744     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2012.93     Document Type: Article

References (55)

1. Anderson SM, Pierce RC (2005). Cocaine-induced alterations in dopamine receptor signaling: implications for reinforcement and reinstatement. Pharmacol Ther 106: 389-403. (Pubitemid 40731541)
2. Awad JA, Johnson RA, Jakobs KH, Schultz G (1983). Interactions of forskolin and adenylate cyclase. Effects on substrate kinetics and protection against inactivation by heat and N-ethylmaleimide. J Biol Chem 258: 2960-2965. (Pubitemid 13130218)
3. Barad M, Bourtchouladze R, Winder DG, Golan H, Kandel E (1998). Rolipram, a type IV-specific phosphodiesterase inhibitor, facilitates the establishment of long-lasting long-term potentiation and improves memory. Proc Natl Acad Sci USA 95: 15020-15025. (Pubitemid 29003749)
4. Carlezon Jr WA, Thome J, Olson VG, Lane-Ladd SB, Brodkin ES, Hiroi N et al (1998). Regulation of cocaine reward by CREB. Science (New York, NY) 282: 2272-2275. (Pubitemid 29004079)
5. Chaperon F, Soubrie P, Puech AJ, Thiebot MH (1998). Involvement of central cannabinoid (CB1) receptors in the establishment of place conditioning in rats. Psychopharmacology 135: 324-332. (Pubitemid 28254837)
6. Chen CC, Yang CH, Huang CC, Hsu KS (2010). Acute stress impairs hippocampal mossy fiber-CA3 long-term potentiation by enhancing cAMP-specific phosphodiesterase 4 activity. Neuropsychopharmacology 35: 1605-1617.
7. Cherry JA, Davis RL (1999). Cyclic AMP phosphodiesterases are localized in regions of the mouse brain associated with reinforcement, movement, and affect. J Comp Neurol 407: 287-301. (Pubitemid 29162777)
8. Chiu CQ, Puente N, Grandes P, Castillo PE (2010). Dopaminergic modulation of endocannabinoid-mediated plasticity at GABAergic synapses in the prefrontal cortex. J Neurosci 30: 7236-7248.
9. Conti M, Richter W, Mehats C, Livera G, Park JY, Jin C (2003). Cyclic AMP-specific PDE4 phosphodiesterases as critical components of cyclic AMP signaling. J Biol Chem 278: 5493-5496. (Pubitemid 36800786)
10. Diamant Z, Spina D (2011). PDE4-inhibitors: a novel, targeted therapy for obstructive airways disease. Pulm Pharmacol Ther 24: 353-360.
11. DiRocco DP, Scheiner ZS, Sindreu CB, Chan GC, Storm DR (2009). A role for calmodulin-stimulated adenylyl cyclases in cocaine sensitization. J Neurosci 29: 2393-2403.
12. Elliott JM, Beveridge TJ (2005). Psychostimulants and monoamine transporters: upsetting the balance. Curr Opin Pharmacol 5: 94-100. (Pubitemid 40124541)
13. Iyo M, Bi Y, Hashimoto K, Inada T, Fukui S (1996). Prevention of methamphetamine-induced behavioral sensitization in rats by a cyclic AMP phosphodiesterase inhibitor, rolipram. Eur J Pharmacol 312: 163-170. (Pubitemid 26325675)
14. Iyo M, Maeda Y, Inada T, Kitao Y, Sasaki H, Fukui S (1995). The effects of a selective cAMP phosphodiesterase inhibitor, rolipram, on methamphetamine-induced behavior. Neuropsychopharmacology 13: 33-39.
15. Janes AC, Kantak KM, Cherry JA (2009). The involvement of type IV phosphodiesterases in cocaine-induced sensitization and subsequent pERK expression in the mouse nucleus accumbens. Psychopharmacology 206: 177-185.
16. Johnson SW, North RA (1992). Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J Physiol 450: 455-468.
17. Jones S, Kauer JA (1999). Amphetamine depresses excitatory synaptic transmission via serotonin receptors in the ventral tegmental area. J Neurosci 19: 9780-9787. (Pubitemid 30226651)
18. Ke H (2004). Implications of PDE4 structure on inhibitor selectivity across PDE families. Int J Impot Res 16(Suppl 1): S24-S27. (Pubitemid 38993080)
19. Knapp CM, Foye MM, Ciraulo DA, Kornetsky C (1999). The type IV phosphodiesterase inhibitors, Ro 20-1724 and rolipram, block the initiation of cocaine self-administration. Pharmacol Biochem Behav 62: 151-158. (Pubitemid 29017768)
20. Larson EB, Graham DL, Arzaga RR, Buzin N, Webb J, Green TA et al (2011). Overexpression of CREB in the nucleus accumbens shell increases cocaine reinforcement in self-administering rats. J Neurosci 31: 16447-16457.
21. Li YF, Cheng YF, Huang Y, Conti M, Wilson SP, O'Donnell JM et al (2011). Phosphodiesterase-4D knock-out and RNA interferencemediated knock-down enhance memory and increase hippocampal neurogenesis via increased cAMP signaling. J Neurosci 31: 172-183.
22. Li YF, Huang Y, Amsdell SL, Xiao L, O'Donnell JM, Zhang HT (2009). Antidepressant-and anxiolytic-like effects of the phosphodiesterase-4 inhibitor rolipram on behavior depend on cyclic AMP response element binding protein-mediated neurogenesis in the hippocampus. Neuropsychopharmacology 34: 2404-2419.
23. Liu QS, Pu L, Poo MM (2005). Repeated cocaine exposure in vivo facilitates LTP induction in midbrain dopamine neurons. Nature 437: 1027-1031. (Pubitemid 41486984)
24. Lu L, Grimm JW, Shaham Y, Hope BT (2003). Molecular neuroadaptations in the accumbens and ventral tegmental area during the first 90 days of forced abstinence from cocaine selfadministration in rats. J Neurochem 85: 1604-1613. (Pubitemid 36702572)
25. Lugnier C (2006). Cyclic nucleotide phosphodiesterase (PDE) superfamily: a new target for the development of specific therapeutic agents. Pharmacol Ther 109: 366-398. (Pubitemid 43132818)
26. Lynch WJ, Taylor JR (2005). Persistent changes in motivation to self-administer cocaine following modulation of cyclic AMPdependent protein kinase A (PKA) activity in the nucleus accumbens. Eur J Neurosci 22: 1214-1220. (Pubitemid 41395386)
27. Maisonneuve IM, Kreek MJ (1994). Acute tolerance to the dopamine response induced by a binge pattern of cocaine administration in male rats: an in vivo microdialysis study. J Pharmacol Exp Ther 268: 916-921. (Pubitemid 24085894)
28. Maldonado R, Saiardi A, Valverde O, Samad TA, Roques BP, Borrelli E (1997). Absence of opiate rewarding effects in mice lacking dopamine D2 receptors. Nature 388: 586-589. (Pubitemid 27340008)
29. Marin MT, Berkow A, Golden SA, Koya E, Planeta CS, Hope BT (2009). Context-specific modulation of cocaine-induced locomotor sensitization and ERK and CREB phosphorylation in the rat nucleus accumbens. Eur J Neurosci 30: 1931-1940.
30. Miller CA, Marshall JF (2005). Molecular substrates for retrieval and reconsolidation of cocaine-associated contextual memory. Neuron 47: 873-884. (Pubitemid 41266953)
31. Miro X, Perez-Torres S, Puigdomenech P, Palacios JM, Mengod G (2002). Differential distribution of PDE4D splice variant mRNAs in rat brain suggests association with specific pathways and presynaptical localization. Synapse 45: 259-269. (Pubitemid 34827559)
32. Mori T, Baba J, Ichimaru Y, Suzuki T (2000). Effects of rolipram, a selective inhibitor of phosphodiesterase 4, on hyperlocomotion induced by several abused drugs in mice. Jpn J Pharmacol 83: 113-118. (Pubitemid 30449739)
33. Navakkode S, Sajikumar S, Frey JU (2004). The type IV-specific phosphodiesterase inhibitor rolipram and its effect on hippocampal long-term potentiation and synaptic tagging. J Neurosci 24: 7740-7744. (Pubitemid 39186829)
34. Nestler EJ (2001). Molecular basis of long-term plasticity underlying addiction. Nat Rev Neurosci 2: 119-128. (Pubitemid 33673366)
35. Neve KA, Seamans JK, Trantham-Davidson H (2004). Dopamine receptor signaling. J Recept Signal Transduct Res 24: 165-205. (Pubitemid 39332216)
36. Olson VG, Zabetian CP, Bolanos CA, Edwards S, Barrot M, Eisch AJ et al (2005). Regulation of drug reward by cAMP response element-binding protein: evidence for two functionally distinct subregions of the ventral tegmental area. J Neurosci 25: 5553-5562. (Pubitemid 40800647)
37. Pan B, Hillard CJ, Liu QS (2008a). Endocannabinoid signaling mediates cocaine-induced inhibitory synaptic plasticity in midbrain dopamine neurons. J Neurosci 28: 1385-1397. (Pubitemid 351231531)
38. Pan B, Hillard CJ, Liu QS (2008b). D2 dopamine receptor activation facilitates endocannabinoid-mediated long-term synaptic depression of GABAergic synaptic transmission in midbrain dopamine neurons via cAMP-protein kinase A signaling. J Neurosci 28: 14018-14030.
39. Pan B, Zhong P, Sun D, Liu QS (2011). Extracellular signalregulated kinase signaling in the ventral tegmental area mediates cocaine-induced synaptic plasticity and rewarding effects. J Neurosci 31: 11244-11255.
40. Paxinos G, Watson C (1986). The Rat Brain in Stereotaxic Coordinates, Compact 3rd edn. Academic Press: Sydney, Orlando.
41. Pliakas AM, Carlson RR, Neve RL, Konradi C, Nestler EJ, Carlezon Jr WA (2001). Altered responsiveness to cocaine and increased immobility in the forced swim test associated with elevated cAMP response element-binding protein expression in nucleus accumbens. J Neurosci 21: 7397-7403. (Pubitemid 32846987)
42. Rutten K, Misner DL, Works M, Blokland A, Novak TJ, Santarelli L et al (2008). Enhanced long-term potentiation and impaired learning in phosphodiesterase 4D-knockout (PDE4D) mice. Eur J Neurosci 28: 625-632. (Pubitemid 352040412)
43. Sakai N, Thome J, Newton SS, Chen J, Kelz MB, Steffen C et al (2002). Inducible and brain region-specific CREB transgenic mice. Mol Pharmacol 61: 1453-1464. (Pubitemid 34575756)
44. Self DW, Genova LM, Hope BT, Barnhart WJ, Spencer JJ, Nestler EJ (1998). Involvement of cAMP-dependent protein kinase in the nucleus accumbens in cocaine self-administration and relapse of cocaine-seeking behavior. J Neurosci 18: 1848-1859. (Pubitemid 28103092)
45. Silva AJ, Kogan JH, Frankland PW, Kida S (1998). CREB and memory. Annu Rev Neurosci 21: 127-148. (Pubitemid 28150661)
46. Swanson LW (1982). The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9: 321-353. (Pubitemid 13225278)
47. Thompson BE, Sachs BD, Kantak KM, Cherry JA (2004). The type IV phosphodiesterase inhibitor rolipram interferes with druginduced conditioned place preference but not immediate early gene induction in mice. Eur J Neurosci 19: 2561-2568. (Pubitemid 38621853)
48. Tolliver BK, Ho LB, Reid MS, Berger SP (1996). Evidence for involvement of ventral tegmental area cyclic AMP systems in behavioral sensitization to psychostimulants. J Pharmacol Exp Ther 278: 411-420. (Pubitemid 27167121)
49. Valjent E, Pascoli V, Svenningsson P, Paul S, Enslen H, Corvol JC et al (2005). Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. Proc Natl Acad Sci USA 102: 491-496. (Pubitemid 40116794)
50. Vecsey CG, Baillie GS, Jaganath D, Havekes R, Daniels A, Wimmer M et al (2009). Sleep deprivation impairs cAMP signalling in the hippocampus. Nature 461: 1122-1125.
51. Walters CL, Blendy JA (2001). Different requirements for cAMP response element binding protein in positive and negative reinforcing properties of drugs of abuse. J Neurosci 21: 9438-9444. (Pubitemid 33096887)
52. Walters CL, Kuo YC, Blendy JA (2003). Differential distribution of CREB in the mesolimbic dopamine reward pathway. J Neurochem 87: 1237-1244. (Pubitemid 37485079)
53. Zhang HT (2009). Cyclic AMP-specific phosphodiesterase-4 as a target for the development of antidepressant drugs. Curr Pharmaceutical Design 15: 1688-1698.
54. Zhang HT, Crissman AM, Dorairaj NR, Chandler LJ, O'Donnell JM (2000). Inhibition of cyclic AMP phosphodiesterase (PDE4) reverses memory deficits associated with NMDA receptor antagonism. Neuropsychopharmacology 23: 198-204. (Pubitemid 30406904)
55. Zhang HT, Zhao Y, Huang Y, Dorairaj NR, Chandler LJ, O'Donnell JM (2004). Inhibition of the phosphodiesterase 4 (PDE4) enzyme reverses memory deficits produced by infusion of the MEK inhibitor U0126 into the CA1 subregion of the rat hippocampus. Neuropsychopharmacology 29: 1432-1439. (Pubitemid 38982235)